1822 • The Journal of Neuroscience, February 25, 2004 • 24(8):1822–1832 Behavioral/Systems/Cognitive Attention to Features Precedes Attention to Locations in Visual Search: Evidence from Electromagnetic Brain Responses in Humans Jens-Max Hopf,1,2 Kai Boelmans,1 Mircea Ariel Schoenfeld,1 Steven J. Luck,3 and Hans-Jochen Heinze1 1Department of Neurology II, Otto-von-Guericke-University, D-39120 Magdeburg, Germany, 2Leibniz-Institute for Neurobiology, D-39120 Magdeburg, Germany, and 3Department of Psychology, University of Iowa, Iowa City, Iowa 52242-1407 Single-unit recordings in macaque extrastriate cortex have shown that attentional selection of nonspatial features can operate in a location-independent manner. Here, we investigated analogous neural correlates at the neural population level in human observers by using simultaneous event-related potential (ERP) and event-related magnetic field (ERMF) recordings. The goals were to determine (1) whether task-relevant features are selected before attention is allocated to the location of the target, and (2) whether this selection reflects the locations of the relevant features. A visual search task was used in which the spatial distribution of nontarget items with attended feature values was varied independently of the location of the target. The presence of task-relevant features in a given location led to a changeinERP/ERMFactivitybeginningϳ140msecafterstimulusonset,withaneuraloriginintheventraloccipito-temporalcortex.This effect was independent of the location of the actual target. This effect was followed by lateralized activity reflecting the allocation of attention to the location of the target (the well known N2pc component), which began at ϳ170 msec poststimulus. Current source localization indicated that the allocation of attention to the location of the target originated in more anterior regions of occipito-temporal cortex anterior than the feature-related effects. These findings suggest that target detection in visual search begins with the detection of task-relevant features, which then allows spatial attention to be allocated to the location of a likely target, which in turn allows the target to be positively identified. Key words: attention; visual; search; featural; spatial; human Introduction (MT) using bilateral moving dot patterns. Attending to a certain Psychophysical and neurophysiological evidence indicates that direction of movement in one visual field also enhanced firing of attention can be focused to spatial locations independent of eye MT cells tuned for that movement direction in the unattended fixations (Posner, 1980; Hillyard and Mu¨nte, 1984; Moran and visual field [for related functional magnetic resonance imaging Desimone, 1985; Motter, 1993; Heinze et al., 1994; Brefczynski (fMRI) evidence, see Saenz et al., 2002]. and DeYoe, 1999). Attention may also be allocated to nonspatial Feature-based attention may be important in visual search, features (Corbetta et al., 1990; O’Craven et al., 1997), and this because it could provide a map of likely target locations (Motter, may occur in a location-independent manner (Motter, 1994; 1994). Feature-based location maps of various kinds have been Treue and Martinez Trujillo, 1999). Motter (1994) has shown postulated in many theories of visual search (Treisman and that the firing rate of color-responsive cells in macaque area V4 is Gelade, 1980; Treisman and Sato, 1990; Wolfe, 1994; Cave, 1999), enhanced when the color of a stimulus in the receptive field of the and behavioral studies have demonstrated that attending to fea- cell matches the color of a previous cue. This effect depended on tures provides access to their spatial locations (Kim and Cave, the presence of the precued color and not on the location of the 1995, 2001; Shui-I and Sperling, 1996). Once relevant features attended items. Treue and Martinez Trujillo (1999) demon- have been located, spatial attention may then be allocated to the strated similar effects in macaque middle temporal visual area locations containing those features (Wolfe et al., 1989; Treisman and Sato, 1990), and this may then allow a suppression of infor- mation from the other locations, improving the perceptual anal- Received July 30, 2003; revised Dec. 4, 2003; accepted Dec. 6, 2003. ysis at attended locations (Chelazzi et al., 1993; Luck et al., This work was supported by Bundesministerium fu¨r Bildung und Forschung Center for Advanced Imaging Grant 1997a). 01GO00202, Grant He1531/3-5 from the Deutsche Forschungs-gemeinschaft to H.-J.H., and Grants MH56877 and MH63001 from the National Institute of Mental Health to S.J.L. We are grateful to E. Du¨zel and A. Richardson- Although this progression from feature- to location-based se- Klavehn for comments on this manuscript. lection is a common idea in theories of attention, there is little Correspondence should be addressed to Dr. Jens-Max Hopf, Department of Neurology II, Otto-von- direct evidence for such progression. Most neurophysiological Guericke-University of Magdeburg, Leipziger Strasse 44, 39120 Magdeburg, Germany. E-mail: studies have examined only feature-based or only location-based [email protected]. DOI:10.1523/JNEUROSCI.3564-03.2004 selection (Motter, 1993, 1994; Luck et al., 1997b, Connor et al., Copyright © 2004 Society for Neuroscience 0270-6474/04/241822-11$15.00/0 1997), and behavioral studies cannot usually provide direct evi- Hopf et al. • Features before Locations in Visual Search J. Neurosci., February 25, 2004 • 24(8):1822–1832 • 1823 dence about the timing of attentional processes. The present study combines event-related potential (ERP)/event-related magnetic field (ERMF) recordings to test the hypothesis that the spatial distribution of task-relevant features is computed rapidly, followed by the focusing of attention onto the object that is most likely to be the target. In ERP studies of visual search, the first index of focusing attention onto the location of the target is N2pc, a negative-going deflection in the N2 time range (180–300 msec) that is largest at posterior scalp sites, contralateral to the location of the attended item (Luck and Hillyard, 1994a,b; Luck et al., 1997a). The N2pc seems to be closely related to modulations of single-unit activity in macaque extrastriate/inferotemporal areas (Chelazzi et al., 1993, 2001) and originates from ventral occipito-temporal cortex in humans (Hopf et al., 2000, 2002a). Our main question was whether the N2pc component would be preceded by activity re- lated to the detection and localization of task-relevant features. Materials and Methods Stimuli and procedure (experiment 1). As illustrated in Figure 1a, each stimulus array consisted of one cluster of C-shaped items (diameter, 0.85°; gap width, 0.6°) in each visual field, centered 2.2° below and 3.6° lateral to the fixation point. Each cluster contained a ring of six blue Cs surrounding, at a distance of 1.5°, either a red C or a green C. A red C was in one cluster, and a green C was in the other, and the side containing a particular color varied randomly from trial to trial. The gap of each central C could be on either the left or right side, varying unpredictably independently. At the beginning of each trial block, the subject was in- structed that either the red C or the green C would be the target for that block (the order alternated across blocks). Subjects were required to report the position of the gap of the target with a two alternative button press of the right hand (left gap ϭ index finger, right gap ϭ middle finger). In this manner, a given stimulus array could serve as a left target array or a right target array, depending on which color was the target for that block. The data were then collapsed across the red target and green target conditions to control for any spatial inhomogeneities attributable to target color. Note that because red and green, but never blue, served as target colors in this experiment, it may be possible that these colors may have gained some significance even when they served as distractors. This may have caused some slight attentional capture toward the nontarget side, an effect that would not be controlled for by collapsing across the red target and green target conditions. However, because this would have affected all four experimental conditions to an equal extent, this would not influence the conclusions that can be drawn from this experiment. The targets in this experiment had two relevant features, namely a Figure 1. a, Stimulus arrays used in the first experiment. Stimuli consisted of arrays of color (which remained constant throughout a trial block) and an orien- C-shaped items placed to the left and right of fixation, with one distinctively colored item in tation (which varied but was always along the horizontal axis). The dis- each field (the red C in the LVF and the green C in the RVF). One of these colors indicated the tractors within a given cluster either shared the same general orientation target for half of the trial blocks, and the other color indicated the target for the other half. as the possible target shapes, with a gap on the left or right side, or did not Distracter items (blue Cs) were placed in both visual fields surrounding the target and the share this orientation, with a gap on the top or bottom. We refer to potential target. The orientation of the distracters was either left–right like the target (ROD) or distractors with the same general orientation as the target category as up–down (irrelevant-orientation